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Article

Physiological Response of Two Typical Plant Species under Combined Pb and Cd Stress in Bioretention Facilities

by
Yongwei Gong
1,*,
Xiaoxiao Lu
1,
Zhihua Zhou
1,2,
Zhuolun Li
1 and
Yanhong Li
3
1
Key Laboratory of Urban Stormwater System and Water Environment, Ministry of Education, Beijing University of Civil Engineering and Architecture, Beijing 100044, China
2
Shandong Green Marching Environmental Engineering Co., Ltd., Jinan 250100, China
3
Beijing Guohuan Tsinghua Environmental Engineering Design & Research Institute Co., Ltd., Beijing 100084, China
*
Author to whom correspondence should be addressed.
Water 2022, 14(23), 3923; https://doi.org/10.3390/w14233923
Submission received: 22 September 2022 / Revised: 22 November 2022 / Accepted: 29 November 2022 / Published: 2 December 2022
(This article belongs to the Special Issue Urban Hydrology and Sustainable Drainage System)
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Abstract

:
Bioretention facilities reduce stormwater runoff and pollutants, but there is a concern that plants in bioretention facilities may absorb heavy metal pollutants from stormwater runoff, which might impair the growth of the plant species. To investigate this issue, stormwater runoff containing various amounts of Pb and Cd heavy metals was used as the irrigation water in a bioretention facility. The low concentrations of Pb and Cd were 0.08 and 0.04 mg/L, and the high values were 0.68 and 0.32 mg/L. The plant heavy metal content and physiological indicators were measured. The indicators were chlorophyll content (CC), net photosynthetic rate (NPR), and transpiration rate (TR). The results showed that the changes in plant chlorophyll content (CC) were highly correlated with changes in the plants’ Pb. Low concentrations of Pb and Cd slightly inhibited the Ginkgo biloba L. and Ligustrum × vicaryi NPRs, the effect was more obvious at high concentrations and the Ligustrum × vicaryi’s NPR decreased from the initial 8.97 μmol CO2/(m2s) to 5.77 μmol CO2/(m2s) under high concentration conditions. Pb and Cd increased the Ginkgo biloba L. and Ligustrum × vicaryi’s TRs, and the effect at low Pb and Cd concentrations was more significant. Under low concentrations of Pb and Cd stress, the Ginkgo biloba L.’s TRs reached 0.63 mmol H2O/(m2s), Ligustrum × vicaryi’s TRs reached 1.30 mmol H2O/(m2s). The TRs of the two plants in the experimental groups remained high throughout the experiment, and there was no significant inhibition. The study found that Pb and Cd in stormwater runoff did affect the physiological function of species to some extent. Different plant species behaved differently in bioretention facilities, but the stormwater runoff did not lead to the death of species. Our study may provide a better understanding of the development of typical plant species in bioretention facilities.

1. Introduction

Heavy metals enter the environment in a variety of ways, including through manmade or natural sources [1,2,3], and are difficult to remove. They accumulate over time, posing a severe threat to the ecological environment [4,5]. Pb is a fuel additive and Cd is produced by tire wear; therefore, Pb and Cd are the most commonly encountered heavy metals in traffic. Heavy metals and other pollutants build up on urban surfaces before being washed away in stormwater runoff [6,7].
The idea of low impact development (LID) was established to mitigate the hazards of stormwater runoff to receiving water bodies. It proposes using decentralized, small-scale source control facilities to collect and purify rainfall runoff from metropolitan areas [8]. In particular, bioretention facilities have compact footprints and are landscaped, which means that they have become popular, small-scale control facilities [9,10]. Bioretention facilities mainly use soil and vegetation to reduce runoff flow and improve water quality [11,12,13]. They also use physical processes, such as adsorption, filtration, sedimentation, and evaporation, to achieve their aims [14,15].
Studies have been undertaken on the effectiveness of heavy metal removal in bioretention facilities. Many studies have shown that the fill and plant components of bioretention facilities play a substantial role in heavy metal removal from stormwater runoff. In phytoremediation, the removal capacity of heavy metals by plant species has been graded. Whether plant species in bioretention facilities were super-enriched plants has not yet been determined, but studies have found that concentrations of heavy metals (Cu, Zn, Mn, and Cd) in the runoff of vegetated plots are all significantly (p < 0.05) lower than those of un-vegetated plots and controls [16], so their ability to remove heavy metals is beyond doubt. In bioretention facilities, (i) plant species differ in their effectiveness, and (ii) native species are more effective than exotic ones [17]. Ying Mei et al. studied the uptake and partitioning of four heavy metals, copper (Cu), cadmium (Cd), lead (Pb), and zinc (Zn), by 30 plant species in North China through pot experiments [18]. The study [19] showed that the adsorption processes could remove up to 89%, 91%, and 91% of Pb, Cr, and Cd, respectively, while plant uptake of these heavy metals was 6%, 5.1%, and 5.2%. Previous studies have shown that when stormwater runoff carrying heavy metals reached the bioretention facility, 88–97% of the heavy metals were removed by the fill layer, 2.0–11.6% were in the outflow, and 0.5–3.3% were absorbed by plants [20]. Heavy metals in plants can come from the soil and/or air deposition [21]. The Cu, Zn, Pb, and Cd in the leaves of coniferous plants may originate from soil, whereas Cu, Zn, Pb, and Cd in the leaves of broad-leaved plants may be derived from significant atmospheric deposition according to an analysis of the relationship between heavy metal concentrations in soil and plant leaves and atmospheric deposition [22]. Plants such as conifers, which can potentially be used to monitor metal levels in the environment, have been investigated as potential bioindicators of environmental pollution [23,24].
Heavy metals have different properties, and different plants and plant sections have different absorption capacities and heavy metal uptake potentials. Although it is widely believed that heavy metals harm plants, the study suggests that moderate quantities of heavy metals may improve some physiological indicators and the growth of plant [25]. Some previous studies have reported that stormwater runoff containing high concentrations of pollutants has no negative or significant effects on the net photosynthetic rate, chlorophyll content, and the electrolyte exudation rate in most plants, and positively affects Iris tectorum Maxim, whereas stormwater runoff containing low concentrations of pollutants has positive or no significant effects on the physiological indicators of herbaceous plants [26]. Perennial ryegrass fading was observed to be slightly different in response to Pb and Cd in a nutrient solution. Fading occurred at Pb concentrations of 0.2 and 0.5 mM, but was more severe at the higher Pb concentration (3.2 mM) [27]. Long-term irrigation with 5 mg/L Cd had no significant harmful effects on poplar tree development. However, the transpiration rate was higher and the photosynthetic rate was lower [28]. Pb buildup in plants has been shown to be caused by elevated Pb levels in the soil, resulting in changes in chloroplast structure and reduced photosynthetic efficiency [29]. Zhang et al. reported that high Cd contamination levels enhanced the chlorophyll content in young leaves but had no effect on mature leaves. It also increased the plant maximum net photosynthetic rate, the light compensation point, and the light saturation point [30]. Ye et al. demonstrated that plants treated with low/medium doses of heavy metals showed physiological alterations, but there were no substantial impacts and they remained viable [31].
Heavy metals from the environment enter bioretention facilities via stormwater runoff. However, some of the heavy metals are hazardous, and the question “to what extent does stormwater runoff containing heavy metals impair plant development when it enters bioretention facilities” remains unanswered. Studies on the effects of heavy metals in stormwater runoff on plant growth are scarce and inconclusive. Therefore, the primary goal of this study is to determine the impact of heavy metal concentrations in stormwater runoff on plant physiological indicators. Pb and Cd are not required for growth and are hazardous at low concentrations [32]. The Pb and Cd in stormwater runoff have been shown to be highly toxic at low levels, can undergo heavy metal accumulation at low levels, and generally have significant effects on plant growth and metabolism in bioretention facilities [33,34,35]. In this study, Pb and Cd were selected as research heavy metals. Two kinds of ornamental species in urban areas, Ginkgo biloba L. and Ligustrum × vicaryi, were selected as research objects. Chlorophyll content, net photosynthetic rate, and transpiration rate were selected as the physiological indicators. The effects of Pb and Cd on physiological indicators of Ginkgo biloba L. and Ligustrum × vicaryi were detected and analyzed.

2. Materials and Methods

2.1. Experimental Site

The experimental site was at the Beijing University of Architecture’s Stormwater Laboratory, Daxing District, Beijing, China. In the study region, the average annual temperature was 12 °C and the average annual rainfall was 626 mm, with most of it falling from July to September, indicating a typical continental monsoon climate.

2.2. Plants and Heavy Metals

The two species used in this study were typically found in northern Chinese urban environments. These were a Ginkgo biloba L. arbor and one shrub, Ligustrum × vicaryi. The two species are decorative perennials with well-developed roots that are tolerant of drought and humidity.
Pb and Cd in road stormwater runoff were the heavy metals investigated in this experiment. The Pb and Cd pollution treatments used in this experiment simulated rainwater runoff with low and high concentrations of the heavy metals. Some scholars have studied the pollutant content of stormwater runoff in Beijing [7,36]; the concentrations of Pb and Cd in road stormwater runoff in Beijing were low and did not exceed CNEQS-SW-II (China National Environmental Quality Standards for Surface Water) which is Pb < 0.05 mg/L, Cd < 0.005 mg/L [7]. Pb(NO3)2 and Cd(NO3)2 were the Pb and Cd sources, the simulated stormwater runoff solution was the tap water solution fused with Pb(NO3)2 and Cd(NO3)2, and the low concentration levels in the rainwater runoff were 0.08 and 0.04 mg/L, respectively. The high concentration levels in the rainwater runoff were eight times those of the low concentrations. The experiment included six experimental treatments: two treatments that simulated low concentrations of heavy metals in rainwater runoff, two treatments that simulated high concentrations of heavy metals in rainwater runoff, and two controls that used tap water (Table 1).
The rainfall data for Beijing over the last 30 years were statistically analyzed to determine the experimental water intake under each treatment in this study and the number of days between water intakes in each month. The field rainfall interval time was 12 h and when the rainfall interval exceeded 12 h, it was defined as two rainfall events. Rainfall of less than 2.0 mm was considered unproductive flow and was not included in the statistical analysis. There have been 317 relevant rainfalls in Beijing over the last 30 years from August to October, with the average number of days between rainfalls in August, September, and October being 6, 8, and 20 days, respectively (Table 2). As a result, this experiment was designed with three groups of inflow intervals. This experiment’s arrangements were as follows: 21 August 2020, 27 August 2020, 2 September 2020, 10 September 2020, 18 September 2020, 26 September 2020, 5 October 2020, 24 October 2020. The simulation experiment ended on 24 October 2020, but measurements of the physiological indicators continued after the end of the experiment. The temperature variation and the maximum radiation variation on the ground during the experiment are shown in Figure 1 and Figure 2, respectively, and the environmental variables remained the same throughout the experiment, except for the artificially set variables.
The ratio of the bioretention facility area to the catchment area was set as 1:3, which was based on the “Sponge city construction technology guide—low impact development rainwater system construction (for trial implementation) and the urban road greening planning and design specifications (CJJ75-97)”. Therefore, the inflow volumes in August, September, and October were 5.45, 5.92, and 5.15 L, respectively (Table 3).
The experimental devices were made entirely of PVC, with a 28 cm water storage layer, a 40 cm filler layer, a geotextile membrane, a 5 cm gravel layer, and a 10 cm base with a 3 cm diameter perforated drainage pipe in the gravel layer. The overall height of the device was 83 cm. The uppermost layer was the water storage layer, which received rainwater runoff. The filler layer was field soil from the Daxing area and was separated from the drainage layer by a geotextile membrane, which acted as a filter layer to prevent the filler from being washed away and entering the drainage layer. The drainage layer, which was composed of gravel with a diameter of around 1 cm and a perforated drainage pipe with an inside diameter of 3 cm, was placed at the bottom of the device (Figure 3).

2.3. Physiological Indicators

Photosynthesis is the most important physiological process occurring in plants. Most studies have demonstrated that plant photosynthesis is very sensitive to heavy metals. Stomatal closure, impaired photosynthetic mechanisms, and disruption of pigment synthesis all lead to a general decrease in photosynthetic efficiency. In this experiment, the plant physiological indicators were chlorophyll content, net photosynthetic rate, and transpiration rate, and it is hoped that the changes in the above physiological indicators will respond to the effects of heavy metals on plants.

2.4. Test of Heavy Metals and Physiological Indicators in Plants

The GFAAS method was used to determine Pb and Cd. The samples were added with 5 mL nitric acid and kept at 160 °C for 4 h in a constant temperature drying oven. Catching the acid to the liquid volume 1 mL, constant volume after cooling. The same procedure was performed with reagent blank experiment, finally using an atomic absorption spectrometer (model: SavantAA) made by GBC Scientific Equipment Pty Ltd. for determination. Only the species in the experimental groups were tested for heavy metals. In one measurement of a physiological index, three leaves were randomly found in a branch of the plant for measurement. For the measurement of the chlorophyll content, the leaves needed to be distinguished into mature leaves and young leaves. The Pb and Cd in the species were analyzed by first cutting the top, middle, and bottom leaves and branches of the species. The young leaf was the second downward leaf from the top of the plant stem and the mature leaf was the sixth leaf [37]. A SPAD-502 Plus chlorophyll meter was used to determine the CC (accuracy: ±1.0 SPAD, precision: 0.1 SPAD, manufacturer: Konica Minolta, Tokyo, Japan). A CI-340 handheld photosynthesis system (manufacturer: CID Bio-Science) was used to assess the NPR [μmol CO2/(m2s)] and TR [mmol H2O/(m2s)]. Calibrating the instruments before the experiment, a plant measured three or six leaves. Each test was administered between 10:00 a.m. and 12:00 p.m. on the test day to ensure data accuracy.

2.5. Data Analysis

The average change rate (ACT) equation was used to elucidate the influence of the heavy metals in the stormwater runoff on plant physiological markers [38].
A C T = ∑ ( M i + 1 M i − 1 ) τ − 1
where   M   is the plant physiological indicators such as CC, NPR, or TR; i is the ith test data; τ is the total number of data.

3. Results and Discussion

3.1. Changes in Chlorophyll Content

The variations in the Ginkgo biloba L. chlorophyll content are shown in Figure 4a. Figure 4a shows that low concentrations of Pb and Cd could slightly alleviate decreases in Ginkgo biloba L. CC. The effect of high concentrations on young leaves was the same as lower concentrations but had a significant inhibitory effect on mature leaves. The CC for G. biloba-T-YL (YL represents young leaves) was generally lower than those for the other treatments, the CC in G. biloba-L-YL was higher than that in G. biloba-T-ML (ML represents mature leaves), and the CC in G. biloba-H-ML was similar to that in G. biloba-T-ML. The mature leaves did not significantly differ among the treatments. The ACT change curve for Ginkgo biloba L. CC shows that CC is less than zero at the end of the incoming water experiment, indicating that the CC in Ginkgo biloba L. do not increase. However, there was a significant increase in the G. biloba-L ACT for CC, indicating that Pb and Cd at low concentrations could partially alleviate the decrease in CC seen in young and mature Ginkgo biloba L. leaves.
The changes in Ligustrum × vicaryi CC are shown in Figure 4b. Low Pb and Cd concentrations inhibited a CC rise in Ligustrum × vicaryi to some degree, but high Pb and Cd concentrations severely inhibited CC increases. The CC in Ligustrum × vicaryi showed an undulating increase, and the increase in mature leaf CC was significantly greater than in young leaves. Furthermore, CC under the L. vicaryi-T treatment was generally higher than that for the L. vicaryi-L and L. vicaryi-H treatments. Low concentrations of Pb and Cd had no effect on the chlorophyll contents of young leaves from the L. vicaryi-L treatment, but significantly inhibited CC increases in mature leaves, and the L. vicaryi-H treatment had a significant inhibitory effect on both young and mature leaves, according to the ACT curves. This indicated that low concentrations of Pb and Cd inhibited chlorophyll increases in Ligustrum × vicaryi to some extent, but high concentrations of Pb and Cd had significant effects. Furthermore, the results showed that chlorophyll levels in Ligustrum × vicaryi were elevated. The ACT results for heavy metal content in Ligustrum × vicaryi showed that the Pb content in Ligustrum × vicaryi decreased at low concentrations and increased at high concentrations, indicating that Pb transport was restricted. However, the higher concentration led to increased plant organ tissue damage, and thus reduced the transport restriction.
The results showed that each plant behaved differently. After analysis, the Pb content in G. biloba-L and G. biloba-H showed increases of 0.0835 mg/kg and 0.0555 mg/kg, respectively, compared to the initial experimental period, and L. vicaryi-L and L. vicaryi-H showed increases of 0.0395 mg/kg and 0.2730 mg/kg, respectively. The chlorophyll changes in both plants were highly correlated with the increase in Pb content. Plants have evolved different resistance mechanisms in response to biotic or abiotic stresses [39]. The toxic excitation effect is a plant phenomenon that can be characterized by an inverse U-shaped curve in which modest concentrations of hazardous chemicals have a stimulatory impact [40]. Honeysuckle has been shown to alleviate the effects of heavy metal stress on plant metabolic disorders by boosting leaf osmoregulatory chemicals and triggering the reactive oxygen species scavenging mechanism under a specified range of heavy metal stresses [41]. Ginkgo biloba L. activated this mechanism to cause harmful excitatory effects in response to low concentrations of Pb and Cd stress in this investigation. In response to the phenomenon of chlorophyll changes occurring in Ligustrum × vicaryi, based on available information, heavy metals can inhibit CC for a variety of reasons, one of which is an increase in the production of chlorophyllase, which disrupts the biosynthesis of chlorophyll and carotenoids and leads to chlorophyll breakdown [42]. The Cd was exclusively found in Ligustrum × vicaryi; therefore, it was probable that Cd stress impaired the photosynthetic organs and damaged the chloroplast ultrastructural components, such as the cystoid membranes [43,44].

3.2. Changes in Net Photosynthetic Rate

Low concentrations of Pb and Cd slightly inhibited the Ginkgo biloba L. and Ligustrum × vicaryi NPRs, and excessive concentrations severely reduced their NPRs (Figure 5a,b). Figure 5a shows that the NPR for Ginkgo biloba L. decreased undulatingly in the G. biloba-T, G. biloba-L, and G. biloba-H treatments, with a maximum net photosynthetic rate of 8.57 μmol CO2/m2s for G. biloba-T, 5.97 μmol CO2/m2s for G. biloba-H and 10.90 μmol CO2/m2s for G. biloba-L. Figure 5c shows that the ACT order for the NPR under the three experimental treatments was G. biloba-L > G. biloba-T > 0 > G. biloba-H, but the device G. biloba-L did not return to its original level. Low concentrations of Pb and Cd impeded the Ginkgo biloba L. NPR.
Figure 5b shows that the NPRs for L. vicaryi-T, L. vicaryi-L, and L. vicaryi-H decreased at first and then increased, but none of them recovered to their initial levels. The maximum net photosynthetic rate occurred on 13 September 2020 and the value for all treatments was 8.97 μmol CO2/m2s. Figure 5c also shows that the ACT for the L. vicaryi-L NPR fell dramatically and was near 0. The ACT for the L. vicaryi-H NPR also decreased, and the ACT order for NPR in the three treatments was L. vicaryi-T > L. vicaryi-H > 0 > L. vicaryi-L. The Pb and Cd caused an overall reduction in the Ligustrum × vicaryi NPR.
In addition to variations in CC, the NPR changes could also be linked to the plant resistance mechanism [45]. Different factors influence the photosynthetic rate, but the two most important are sunlight and CO2 [46]. Heavy metals impair photosynthesis at the whole plant level by reducing stomatal conductance and photosynthetic pigment levels. They also indirectly affect chloroplast activity and other metabolic activities [47]. Pb enters the cells and has a variety of harmful effects on plant physiological and biochemical processes, resulting in cellular abnormalities that disturb normal physiological activities. These changes lead to decreased growth and metabolism, membrane disruption, and impaired photosynthesis [48,49]. Cadmium (0 and 5 mg/L) also has been shown to dramatically lower stomatal conductance and the plant photosynthetic rate [28].
A comparison between the two plants showed that the NPRs for Ginkgo biloba L. and Ligustrum × vicaryi were related to the Pb and Cd concentrations. The analysis suggested that, in addition to the inconsistency among different plants to different heavy metal treatments, the co-existence of Pb and Cd, might also have a significant effect. Pb and Cd were not detected in the two plants several times (Table 4).
It suggests that the greatest barrier to the entry of heavy metal ions into plant tissues was the physicochemical features of the plant root system [50]. The root uptake system means that root cells in plants can actively avoid Cd ions [50,51]. A second possibility is that heavy metals are retained in the roots of many plants, reducing their transfer to the aboveground tissues [52,53,54]. It has been found that the translocation of some specific heavy metals, such as Pb and especially Cd, was limited [54]. A third possibility is that coexisting elements reduced Cd absorption by plant roots. It has been found that the coexisting elements restrict the Cd uptake by maize roots, and their inhibitory capacity connects to the chemical characteristics of each element [55]. However, our trials did not continue throughout the year, which limited the number of accessible testing dates and could have resulted in lower Cd uptake recordings by Ginkgo biloba L. and Ligustrum × vicaryi.

3.3. Changes in Transpiration Rate

Pb and Cd led to an increase in the Ginkgo biloba L. and Ligustrum × vicaryi TR, and the effects of low Pb and Cd concentrations were more significant (Figure 6a,b). According to Figure 6a, the G. biloba-T, G. biloba-L, and G. biloba-H treatment TRs showed relatively large fluctuations, and the maximum values of the TRs for G. biloba-T, G. biloba-L, and G. biloba-H all occurred on the 24 October 2020. According to Figure 6c, the ACT order for the G. biloba-T, G. biloba-L, and G. biloba-H TRs was G. biloba-L > G. biloba-H > G. biloba-T > 0, indicating that Pb and Cd increased the Ginkgo biloba L. TR. Figure 6b shows that the L. vicaryi-T, L. vicaryi-L, and L. vicaryi-H TRs had similar trends, showing an increase, a decrease, and then an increase, with a maximum TR of 1 mmol H2O/m2s for L. vicaryi-T and 1.4 mmol H2O/m2s for L. vicaryi-L and L. vicaryi-H. Figure 6c shows that the ACT order for the L. vicaryi-T, L. vicaryi-L, and L. vicaryi-H TRs is L. vicaryi-L > L. vicaryi-H > L. vicaryi-T > 0, which indicates that Pb and Cd increase the Ligustrum × vicaryi TR and that the effect of the low Pb and Cd concentrations is more significant. Changes in the transpiration rate of plants resembled a toxic excitation effect, which is a plant phenomenon that can be characterized by an inverse U-shaped curve in which modest concentrations of hazardous chemicals had a stimulatory impact [40].
Figure 6a and Table 4 show that the experimental treatment changes are approximately the same. Both figures show that the TR and Pb content first increased and then decreased over time in the two plants. Figure 6b and Table 4 show that the changes are relatively consistent over time. However, the correlation analysis showed that the changes in the plant physiological indicators did not significantly correlate with the changes in plant heavy metal contents. Explaining the reasons for this, the heavy metal contents in the plants were relatively small. Furthermore, the insignificant correlation also indicated that the impact of heavy metals in the stormwater runoff on plants in bioretention facilities was relatively small and that the plants could withstand the heavy metal loading. The TRs of the two plants improved when Pb and Cd were present, regardless of the Pb and Cd concentrations, and the effect was more noticeable for both plants at low concentrations. This showed that Pb and Cd had a positive and stimulating effect on plant TR.

4. Conclusions

This study examined the physiological responses of Ginkgo biloba L. and Ligustrum × vicaryi in bioretention facilities to compound heavy metals by simulating Pb and Cd concentrations in stormwater runoff and detecting changes in the physiological indicators for Ginkgo biloba L. and Ligustrum × vicaryi. Overall, the stormwater runoff containing low and high concentrations of Pb and Cd did not influence the mortality of plant species when directly contacting plant species. In fact, according to the results of the study, they did affect the physiological functions of plant species in bioretention facilities to some extent, but not all of these effects were negative. In the case of stormwater runoff containing low concentrations of Pb and Cd, bioretention facility plants showed positive changes compared to the blank control group, especially for the Ginkgo biloba L. species. For stormwater runoff with high concentrations of Pb and Cd, bioretention plants performed less well compared to the blank control group, and this performance was even more pronounced on Ligustrum × vicaryi. The stormwater runoff with high concentrations of Pb and Cd harmed the growth and development of bioretention facilities plants to some extent. Specific conclusions were as follows:
(1)
Low concentrations of Pb and Cd helped to prevent chlorophyll loss in Ginkgo biloba L. leaves, whereas high Pb and Cd concentrations may help prevent chlorophyll loss in young leaves but aggravate chlorophyll loss in mature leaves. Regardless of the concentrations, Pb and Cd reduced the CC increase in Ligustrum × vicaryi leaves. The changes in plant CC were highly correlated with the changes in plant Pb content.
(2)
Low concentrations of Pb and Cd slightly inhibited the Ginkgo biloba L. and Ligustrum × vicaryi NPRs, whereas excessive concentrations severely reduced the NPR.
(3)
Pb and cadmium increased the Ginkgo biloba L. and Ligustrum × vicaryi TRs and the effect of low Pb and Cd concentrations was more significant.

Author Contributions

Conceptualization, Y.L. and Z.L.; methodology, Y.G.; validation, X.L. and Z.Z.; formal analysis, X.L. and Z.Z.; investigation, X.L. and Z.Z.; resources, Y.G.; data curation, X.L. and Z.Z.; writing—original draft preparation, X.L.; writing—review and editing, Y.G.; visualization, Y.G.; supervision, Y.G.; All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the National Natural Science Foundation of China (51879004), the Major Science and Technology Program for Water Pollution Control and Treatment (2017ZX07403001), and the Basic Research Fund of Beijing University of Civil Engineering and Architecture (X20145 and X20160).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study is available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Huang, Q.; Liu, X.; Zhang, Q.; Qiao, Y.; Su, D.; Jiang, R.; Rui, Y.; Li, H. Application of ICP-MS and AFS to detecting heavy metals in Phosphorus fertilizers. Spectrosc. Spectr. Anal. 2014, 34, 1403–1406. [Google Scholar]
  2. Jiao, B.; Xu, G.; Li, D.; Luo, J.; Yang, K. Hazards of heavy metals in coal. Disaster Adv. 2012, 5, 1812–1818. [Google Scholar]
  3. Sansalone, J.J.; Buchberger, S.G. An infiltration device as a best management practice for immobilizing heavy-metals in urban highway runoff. Water Sci. Technol. 1995, 32, 119–125. [Google Scholar] [CrossRef]
  4. Belluck, D.A.; Lynott, W.J.; Benjamin, S.L. Human and ecological health risks from heavy metals and other substances released to the environment from metal shredders. In Cytotoxic, Mutagenic and Carcinogenic Potential of Heavy Metals Related to Human Environment; Springer: Dordrecht, The Netherlands, 1997; pp. 363–373. [Google Scholar]
  5. Zhuo, H.; Fu, S.; Liu, H.; Song, H.; Ren, L. Soil heavy metal contamination and health risk assessment associated with development zones in Shandong, China. Environ. Sci. Pollut. Res. 2019, 26, 30016–30028. [Google Scholar] [CrossRef] [PubMed]
  6. Reddy, K.R.; Dastgheibi, S.; Cameselle, C. Removal kinetics of heavy metals and nutrients from stormwater by different filter materials. Water Air Soil Pollut. 2020, 231, 530. [Google Scholar] [CrossRef]
  7. Shajib, M.T.I.; Hansen, H.C.B.; Liang, T.; Holm, P.E. Metals in surface specific urban runoff in Beijing. Environ. Pollut. 2019, 248, 584–598. [Google Scholar] [CrossRef] [PubMed]
  8. Ma, Y.; He, W.; Zhao, H.; Zhao, J.; Wu, X.; Wu, W.; Li, X.; Yin, C. Influence of Low Impact Development practices on urban diffuse pollutant transport process at catchment scale. J. Clean. Prod. 2019, 213, 357–364. [Google Scholar] [CrossRef]
  9. Vijayaraghavan, K.; Biswal, B.K.; Adam, M.G.; Soh, S.H.; Tsen-Tieng, D.L.; Davis, A.P.; Chew, S.H.; Tan, P.Y.; Babovic, V.; Balasubramanian, R. Bioretention systems for stormwater management: Recent advances and future prospects. J. Environ. Manag. 2021, 292, 112766. [Google Scholar] [CrossRef]
  10. Zhang, L.; Lu, Q.; Ding, Y.; Wu, J. A procedure to design road bioretention soil media based on runoff reduction and pollutant removal performance. J. Clean. Prod. 2021, 287, 125524. [Google Scholar] [CrossRef]
  11. Davis, A.P.; Hunt, W.F.; Traver, R.G.; Clar, M. Bioretention technology: Overview of current practice and future needs. J. Environ. Eng. 2009, 135, 109–117. [Google Scholar] [CrossRef]
  12. Hatt, B.E.; Fletcher, T.D.; Deletic, A. Hydrologic and pollutant removal performance of stormwater biofiltration systems at the field scale. J. Hydrol. 2009, 365, 310–321. [Google Scholar] [CrossRef]
  13. Kong, Z.; Song, Y.; Shao, Z.; Chai, H. Biochar-pyrite bi-layer bioretention system for dissolved nutrient treatment and by-product generation control under various stormwater conditions. Water Res. 2021, 206, 117737. [Google Scholar] [CrossRef]
  14. Egemose, S.; Sonderup, M.J.; Grudinina, A.; Hansen, A.S.; Flindt, M.R. Heavy metal composition in stormwater and retention in ponds dependent on pond age, design and catchment type. Environ. Technol. 2015, 36, 959–969. [Google Scholar] [CrossRef]
  15. Wadzuk, B.M.; Hickman, J.M.; Traver, R.G. Understanding the role of evapotranspiration in bioretention: Mesocosm study. J. Sustain. Water Built Environ. 2015, 1. [Google Scholar] [CrossRef]
  16. Park, S.Y.; Oh, D.K.; Lee, S.Y.; Yeum, K.J.; Yoon, Y.H.; Ju, J.H. Combined Effects of Substrate Depth and Vegetation of Green Roofs on Runoff and Phytoremediation under Heavy Rain. Water 2022, 14, 2792. [Google Scholar] [CrossRef]
  17. Dagenais, D.; Brisson, J.; Fletcher, T.D. The role of plants in bioretention systems; does the science underpin current guidance? Ecol. Eng. 2018, 120, 532–545. [Google Scholar] [CrossRef]
  18. Mei, Y.; Zhou, H.; Gao, L.; Zuo, Y.M.; Wei, K.H.; Cui, N.Q. Accumulation of Cu, Cd, Pb, Zn and total P from synthetic stormwater in 30 bioretention plants. Environ. Sci. Pollut. Res. 2020, 27, 19888–19900. [Google Scholar] [CrossRef]
  19. Mohammed, A.; Babatunde, A.O. Modelling heavy metals transformation in vertical flow constructed wetlands. Ecol. Model. 2017, 354, 62–71. [Google Scholar] [CrossRef]
  20. Sun, X.; Davis, A.P. Heavy metal fates in laboratory bioretention systems. Chemosphere 2007, 66, 1601–1609. [Google Scholar] [CrossRef]
  21. Shahid, M.; Dumat, C.; Khalid, S.; Schreck, E.; Xiong, T.T.; Niazi, N.K. Foliar heavy metal uptake, toxicity and detoxification in plants: A comparison of foliar and root metal uptake. J. Hazard. Mater. 2017, 325, 36–58. [Google Scholar] [CrossRef] [Green Version]
  22. Liang, J.; Fang, H.; Zhang, T.; Wang, X.; Liu, Y. Heavy metal in leaves of twelve plant species from seven different areas in Shanghai, China. Urban For. Urban Green. 2017, 27, 390–398. [Google Scholar] [CrossRef]
  23. Ceburnis, D.; Steinnes, E. Conifer needles as biomonitors of atmospheric heavy metal deposition: Comparison with mosses and precipitation, role of the canopy. Atmos. Environ. 2000, 34, 4265–4271. [Google Scholar] [CrossRef]
  24. Gandois, L.; Probst, A. Localisation and mobility of trace metal in silver fir needles. Chemosphere 2012, 87, 204–210. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Alaboudi, K.A.; Ahmed, B.; Brodie, G. Phytoremediation of Pb and Cd contaminated soils by using sunflower (Helianthus annuus) plant. Ann. Agric. Sci. 2018, 63, 123–127. [Google Scholar] [CrossRef]
  26. Gong, Y.; Hao, Y.; Li, J.; Li, H.; Shen, Z.; Wang, W.; Wang, S. The effects of rainfall runoff pollutants on plant physiology in a bioretention system based on pilot experiments. Sustainability 2019, 11, 6402. [Google Scholar] [CrossRef] [Green Version]
  27. Lou, Y.; Luo, H.; Hu, T.; Li, H.; Fu, J. Toxic effects, uptake, and translocation of Cd and Pb in perennial ryegrass. Ecotoxicology 2013, 22, 207–214. [Google Scholar] [CrossRef]
  28. Hatamian, M.; Nejad, A.R.; Kafi, M.; Souri, M.K.; Shahbazi, K. Nitrate improves hackberry seedling growth under cadmium application. Heliyon 2020, 6, e03247. [Google Scholar] [CrossRef] [Green Version]
  29. Kushwaha, A.; Hans, N.; Kumar, S.; Rani, R. A critical review on speciation, mobilization and toxicity of lead in soil microbe-plant system and bioremediation strategies. Ecotoxicol. Environ. Saf. 2018, 147, 1035–1045. [Google Scholar] [CrossRef]
  30. Zhang, X.; Gao, B.; Xia, H. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotoxicol. Environ. Saf. 2014, 106, 102–108. [Google Scholar] [CrossRef]
  31. Ye, Z.; Baker, A.J.M.; Wong, M.; Willis, A.J. Copper tolerance, uptake and accumulation by phragmites australis. Chemosphere 2003, 50, 795–800. [Google Scholar] [CrossRef] [PubMed]
  32. Beltrame, M.O.; De Marco, S.G.; Marcovecchio, J.E. Dissolved and particulate heavy metals distribution in coastal lagoons. A case study from Mar Chiquita Lagoon, Argentina. Estuar. Coast. Shelf Sci. 2009, 85, 45–56. [Google Scholar] [CrossRef]
  33. Kastori, R.; Petrovic, M.; Petrovic, N. EFFECT of excess Lead, Cadmium, Copper, and Zinc on water relations in sunflower. J. Plant Nutr. 1992, 15, 2427–2439. [Google Scholar] [CrossRef]
  34. Puig, S.; Thiele, D.J. Molecular mechanisms of copper uptake and distribution. Curr. Opin. Chem. Biol. 2002, 6, 171–180. [Google Scholar] [CrossRef]
  35. Zhang, X.; Yang, H.; Cui, Z. Evaluation and analysis of soil migration and distribution characteristics of heavy metals in iron tailings. J. Clean. Prod. 2018, 172, 475–480. [Google Scholar] [CrossRef]
  36. Zhao, H.; Li, X.; Wang, X.; Tian, D. Grain size distribution of road-deposited sediment and its contribution to heavy metal pollution in urban runoff in Beijing, China. J. Hazard. Mater. 2010, 183, 203–210. [Google Scholar] [CrossRef]
  37. Zhang, X.; Zhang, X.; Gao, B.; Li, Z.; Xia, H.; Li, H.; Li, J. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of an energy crop, king grass (Pennisetum americanum x P. purpureum). Biomass Bioenergy 2014, 67, 179–187. [Google Scholar] [CrossRef]
  38. Zhang, P.; Wang, Y.L.; Liang, L.K.; Li, X.; Duan, Q.T. Short-Term Wind Power Prediction Using GA-BP Neural Network Based on DBSCAN Algorithm Outlier Identification. Processes 2020, 8, 157. [Google Scholar] [CrossRef] [Green Version]
  39. DalCorso, G.; Farinati, S.; Furini, A. Regulatory networks of cadmium stress in plants. Plant Signal. Behav. 2010, 5, 663–667. [Google Scholar] [CrossRef]
  40. Malkowski, E.; Sitko, K.; Szopinski, M.; Gieron, Z.; Pogrzeba, M.; Kalaji, H.M.; Zieleznik-Rusinowska, P. Hormesis in plants: The role of oxidative stress, auxins and photosynthesis in corn treated with Cd or Pb. Int. J. Mol. Sci. 2020, 21, 2099. [Google Scholar] [CrossRef] [Green Version]
  41. Mao, X.; Xu, X.; Chen, L. Effect of heavy metal Pb and Cd stress on physiological characteristics of Japanese Honeysuckle. Appl. Ecol. Environ. Res. 2019, 17, 6415–6427. [Google Scholar] [CrossRef]
  42. Saleh, S.R.; Kandeel, M.M.; Ghareeb, D.; Ghoneim, T.M.; Talha, N.I.; Alaoui-Sosse, B.; Aleya, L.; Abdel-Daim, M.M. Wheat biological responses to stress caused by cadmium, nickel and lead. Sci. Total Environ. 2020, 706, 136013. [Google Scholar] [CrossRef] [PubMed]
  43. Bahmani, R.; Modareszadeh, M.; Bihamta, M.R. Genotypic variation for cadmium tolerance in common bean (Phaseolus vulgaris L.). Ecotoxicol. Environ. Saf. 2020, 190, 110178. [Google Scholar] [CrossRef] [PubMed]
  44. Dobrikova, A.G.; Apostolova, E.L. Chapter 11—Damage and protection of the photosynthetic apparatus under Cadmium stress. In Cadmium Toxicity and Tolerance in Plants; Hasanuzzaman, M., Prasad, M.N.V., Fujita, M., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 275–298. [Google Scholar]
  45. Parys, E.; Wasilewska, W.; Siedlecka, M.; Zienkiewicz, M.; Drozak, A.; Romanowska, E. Metabolic responses to Lead of metallicolous and nonmetallicolous populations of armeria maritima. Arch. Environ. Contam. Toxicol. 2014, 67, 565–577. [Google Scholar] [CrossRef]
  46. Zhou, Y.; Han, S. Photosynthetic response and stomatal behaviour of Pinus koraiensis during the fourth year of exposure to elevated CO2 concentration. Photosynthetica 2005, 43, 445–449. [Google Scholar] [CrossRef]
  47. Sheoran, I.S.; Aggarwal, N.; Singh, R. Effects of cadmium and nickel on in vivo carbon dioxide exchange rate of pigeon pea (Cajanus cajan L.). Plant Soil 1990, 129, 243–249. [Google Scholar] [CrossRef]
  48. Ahmad, M.S.A.; Hussain, M.; Ijaz, S.; Alvi, A.K. Photosynthetic performance of two mung bean (Vigna radiata) cultivars under lead and copper stress. Int. J. Agric. Biol. 2008, 10, 167–172. [Google Scholar]
  49. Sharma, P.; Dubey, R.S. Lead toxicity in plants. Braz. J. Plant Physiol. 2005, 17, 35–52. [Google Scholar] [CrossRef] [Green Version]
  50. White, P.J. Chapter 2—Ion uptake mechanisms of individual cells and roots: Short-distance transport. In Marschner’s Mineral Nutrition of Higher Plants, 3rd ed.; Marschner, P., Ed.; Academic Press: San Diego, CA, USA, 2012; pp. 7–47. [Google Scholar]
  51. Cobbett, C.; Goldsbrough, P. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 2002, 53, 159–182. [Google Scholar] [CrossRef] [Green Version]
  52. Bose, S.; Bhattacharyya, A.K. Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 2008, 70, 1264–1272. [Google Scholar] [CrossRef]
  53. Ghosh, R.; Roy, S. Cadmium Toxicity in Plants: Unveiling the Physicochemical and Molecular Aspects; Academic Press: Cambridge, MA, USA, 2019; pp. 223–246. [Google Scholar]
  54. Lux, A.; Martinka, M.; Vaculik, M.; White, P.J. Root responses to cadmium in the rhizosphere: A review. J. Exp. Bot. 2011, 62, 21–37. [Google Scholar] [CrossRef] [Green Version]
  55. Sterckeman, T.; Redjala, T.; Morel, J.L. Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. Environ. Exp. Bot. 2011, 74, 131–139. [Google Scholar] [CrossRef]
Water 14 03923 g001 550
Figure 1. Changes in temperature during the experiment.
Figure 1. Changes in temperature during the experiment.
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Water 14 03923 g002 550
Figure 2. Changes in surface maximum radiation during the experiment.
Figure 2. Changes in surface maximum radiation during the experiment.
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Water 14 03923 g003 550
Figure 3. Actual view and cross-section of the experimental device.
Figure 3. Actual view and cross-section of the experimental device.
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Water 14 03923 g004 550
Figure 4. Changes in (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi chlorophyll contents, n = 3; and (c) chlorophyll content ACT in the plants.
Figure 4. Changes in (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi chlorophyll contents, n = 3; and (c) chlorophyll content ACT in the plants.
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Water 14 03923 g005 550
Figure 5. Changes in the (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi net photosynthetic rates, error bar represented the measurement error of n leaf physiological index of the same plant, n = 3; and (c) ACT for the net photosynthetic rate.
Figure 5. Changes in the (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi net photosynthetic rates, error bar represented the measurement error of n leaf physiological index of the same plant, n = 3; and (c) ACT for the net photosynthetic rate.
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Water 14 03923 g006 550
Figure 6. Changes in the (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi transpiration rates; error bar represented the measurement error of n leaf physiological index of the same plant, n = 3; and (c) ACT for the plant transpiration rate.
Figure 6. Changes in the (a) Ginkgo biloba L. and (b) Ligustrum × vicaryi transpiration rates; error bar represented the measurement error of n leaf physiological index of the same plant, n = 3; and (c) ACT for the plant transpiration rate.
Water 14 03923 g006
Table
Table 1. Experimental treatments information and number.
Table 1. Experimental treatments information and number.
ClassificationInflowPlantsDevice Codes
Experimental groupsrunoff with low concentrations of heavy metalsGinkgo biloba L.G. biloba-L
Ligustrum × vicaryiL. vicaryi-L
runoff with high concentrations of heavy metalsGinkgo biloba L.G. biloba-H
Ligustrum × vicaryiL. vicaryi-H
Control grouptap waterGinkgo biloba L.G. biloba-T
Ligustrum × vicaryiL. vicaryi-T
Note(s): n = 3.
Table
Table 2. Annual rainfall statistics in August, September, and October.
Table 2. Annual rainfall statistics in August, September, and October.
MonthRainfall FrequencyAverage Monthly FrequencyRainfall Totals (mm)Average Rainfall per Event (mm)Rainfall Interval (Days)
August1595.301547.719.735.85
September1113.701174.3210.588.11
October471.57432.259.2019.79
Table
Table 3. Experimental water inflow parameters for August, September, and October.
Table 3. Experimental water inflow parameters for August, September, and October.
MonthRainfall Interval (Days)Average Rainfall per Event (mm)Inflow Volume (L)
August69.735.45
September810.585.92
October209.205.15
Table
Table 4. Heavy metal level in plants based on single factor index (mg/kg).
Table 4. Heavy metal level in plants based on single factor index (mg/kg).
TimePbCd
G. biloba-LG. biloba-HL. vicaryi-LL. vicaryi-HG. biloba-LG. biloba-HL. vicaryi-LL. vicaryi-H
08/20/20200.1185 ± 0.0021 a0.1625 ± 0.00350.1870 ± 0.00840.1450 ± 0.0028----0.01825 ± 0.00080.0154 ± 0.0004
09/05/20200.1435 ± 0.00070.1405 ± 0.00350.1575 ± 0.00210.1015 ± 0.00070.0069 ± 0.00030.0069 ± 0.000020.01395 ± 0.00040.008515 ± 0.00004
09/21/20200.1855 ± 0.00070.1465 ± 0.00640.1030 ± 0.00140.1305 ± 0.0007----0.008175 ± 0.00010.0108 ± 0.0001
10/18/20200.2310 ± 0.015560.2610 ± 0.00710.2825 ± 0.00770.2895 ± 0.01480.0024 ± 0.00060.0019 ± 0.00010.003775 ± 0.00010.004795 ± 0.0003
11/03/20200.3095 ± 0.00070.2610 ± 0.00140.1870 ± 0.00280.1495 ± 0.00350.0036 ± 0.0005------
12/10/20200.2020 ± 0.00140.2180 ± 0.00140.2265 ± 0.00350.4180 ± 0.0113--0.0072 ± 0.00040.0142 ± 0.00010.02195 ± 0.0002
Note(s): a Single factor index data are mean ± SD.—Indicates that the detection value is lower than the detection limit. The detection limit of Pb is 0.02 mg/kg, the limit of quantification is 0.04 mg/kg; the detection limit of Cd is 0.001 mg/kg, the limit of quantification is 0.003 mg/kg.
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Gong, Y.; Lu, X.; Zhou, Z.; Li, Z.; Li, Y. Physiological Response of Two Typical Plant Species under Combined Pb and Cd Stress in Bioretention Facilities. Water 2022, 14, 3923. https://doi.org/10.3390/w14233923

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Gong Y, Lu X, Zhou Z, Li Z, Li Y. Physiological Response of Two Typical Plant Species under Combined Pb and Cd Stress in Bioretention Facilities. Water. 2022; 14(23):3923. https://doi.org/10.3390/w14233923

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Gong, Yongwei, Xiaoxiao Lu, Zhihua Zhou, Zhuolun Li, and Yanhong Li. 2022. "Physiological Response of Two Typical Plant Species under Combined Pb and Cd Stress in Bioretention Facilities" Water 14, no. 23: 3923. https://doi.org/10.3390/w14233923

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